Abstract
Entomopathogenic fungi are considered promising microbial control agents for the control of post-harvest insects, and their evaluation for this purpose has lately attracted a significant amount of research. They are naturally occurring, environmentally safe organisms that infect insects by contact. Insect fungal pathogens have a broad spectrum of hosts, can be mass-produced easily, rapidly and economically and can be applied with the same technical means as conventional contact insecticides. In this context, the most studied fungal species for the control of stored-product insect species are Beauveria bassiana and Metarhizium anisopliae. Both fungal species have a wide host range and have been tested against most of the major stored-product insect pests. The effect of biotic and abiotic factors on the virulence and success of entomopathogenic fungi in storage insect control, as well as the combined application of these agents with other pest control technologies, is reviewed here. Temperature and relative humidity influence the efficacy of entomopathogenic fungi, often with variable results, whereas the combined use of entomopathogenic fungi with diatomaceous earth in many cases has a synergistic or additive effect. Alternative methods of entomopathogenic fungi application, based on the lure-and-kill approach, are proposed, and future challenges for the use of entomopathogenic fungi against stored-product insects are highlighted.
Similar content being viewed by others
References
Acheampong MA, Cornelius EW, Eziah VY, Fening KO, Luke B, Moore D, Clottey VA, Storm C, Potin O (2016) Beauveria bassiana affects immature stage development of Prostephanus truncatus (Coleoptera: Bostrichidae) in stored maize. Biocontrol Sci Techn 26:1516–1525
Adane K, Moore D, Archer SA (1996) Preliminary studies on the use of Beauueria bassiana to control Sitophilus zeamais (Coleoptera: Curculionidae) in the laboratory. J Stored Prod Res 32:105–113
Adler C (2010) Physical control of stored product insects. In: Reichmuth C, Schoeller M (eds) International European symposium on stored product protection “Stress on chemical products”. Julius-Kühn-Archive, Berlin, pp 33–35
Akbar W, Lord JC, Nechols JR, Howard RW (2004) Diatomaceous earth increases the efficacy of Beauveria bassiana against Tribolium castaneum larvae and increases conidia attachment. J Econ Entomol 97:273–280
Akbar W, Lord JC, Nechols JR, Loughin TM (2005) Efficacy of Beauveria bassiana for red flour beetle when applied with plant essential oils or in mineral oil and organosilicone carriers. J Econ Entomol 98:683–688
Athanassiou CG, Steenberg T (2007) Insecticidal effect of Beauveria bassiana (Balsamo) Vuillemin (Ascomycota: Hypocreales) in combination with three diatomaceous earth formulations against Sitophilus granarius (L.) (Coleoptera: Curculionidae). Biol Control 40:411–416
Athanassiou CG, Steenberg T, Kavallieratos NG (2006) Insecticidal effect of diatomaceous earth applied alone or in combination with Beauveria bassiana and beta cyfluthrin against Sitophilus granarius on stored wheat. IOBC/WPRS 30:25–36
Athanassiou CG, Kavallieratos NG, Vayias BJ, Tsakiri JB, Mikeli NH, Meletsis CM, Tomanović Z (2008) Persistence and efficacy of Metarhizium anisopliae (Metschnikoff) Sorokin (Deuteromycotina: Hyphomycetes) and diatomaceous earth against Sitophilus oryzae (L.) (Coleoptera: Curculionidae) and Rhyzopertha dominica (F.) (Coleoptera: Bostrychidae) on wheat and maize. Crop Prot 27:1303–1311
Athanassiou CG, Vassilakos NT, Dutton AC, Jeesop N, Sherwood D, Pease G, Brglez A, Storm C, Trdan S (2016) Combining electrostatic powder with an insecticide: effect on stored product beetles and on the commodity. Pest Manag Sci. doi:10.1002/ps.4255
Baker K, Cook RJ (1982) Biological control of plant pathogens. The American Phytopathological Society, St. Paul
Barra P, Rosso L, Nesci A, Etcheverry M (2013) Isolation and identification of entomopathogenic fungi and their evaluation against Tribolium confusum, Sitophilus zeamais, and Rhyzopertha dominica in stored maize. J Pest Sci 86:217–226
Batta YA (2004) Control of rice weevil (Sitophilus oryzae L., Coleoptera: Curculionidae) with various formulations of Metarhizium anisopliae. Crop Prot 23:103–108
Batta YA (2005) Control of the lesser grain borer (Rhyzopertha dominica (F.), Coleoptera: Bostrichidae) by treatments with residual formulations of Metarhizium anisopliae (Metschnikoff) Sorokin (Deuteromycotina: Hyphomycetes). J Stored Prod Res 41:221–229
Batta YA (2008) Control of main stored-grain insects with new formulations of entomopathogenic fungi in diatomaceous earth dusts. Int J Food Eng 4:9
Batta YA (2016a) Recent advances in formulation and application of entomopathogenic fungi for biocontrol of stored grain insects. Biocontrol Sci Technol 26:1171–1183
Batta YA (2016b) Invert emulsion: Method of preparation and application as proper formulation of entomopathogenic fungi. MethodsX 3:119–127
Batta YA, Murdoch G, Mansfield S (2010) Investigations into the formulation and efficacy of entomopathogenic fungi against larvae of yellow mealworm (Tenebrio molitor L., Coleoptera: Tenebrionidae). Gen Appl Entomol 39:5–8
Baxter IH (2008) Entomopathogen based autodissemination for the control of Plodia interpunctella (Hübner)—an examination of the critical components. Ph.D. Thesis, University of Southampton, p 149
Baxter IH, Howard N, Armsworth CG, Barton LEE, Jackson C (2008) The potential of two electrostatic powders as the basis for an autodissemination control method of Plodia interpunctella (Hübner). J Stored Prod Res 44:152–161
Berliner E (1915) Über die Schlaffsucht der Mehlmottenraupe (Ephestia kühniella Zell.) und ihren Erreger Bacillus thuringiensis n. sp. Zeitschrift für Angewandte Entomologie 2:29–56
Bourassa CC, Vincent CJ, Borgemeister C, Mauffette Y (2001) Effect of entomopathogenic hyphomycetes against the larger grain borer, Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae), and its predator, Teretriosoma nigrescens Lewis (Coleoptera: Histeridae). J Invertebr Pathol 77:75–77
Brower JH, Smith L, Vail PV, Flinn PW (1996) Biological control. In: Subramanyam BH, Hagstrum DW (eds) Integrated management of insects in stored products. Marcel Dekker, New York, pp 223–286
Buchwald J, Berliner E (1910) Habrobracon hebetor Say in Bundesgenosse im Kampf gegen die Mehlmotte. Zeitschridt für das Gesamte Getreidewesen 2:1–4
Burges HD (1981) Safety, safety testing and quality control of microbial pesticides. In: Burges HD (ed) Microbial control of pests and plant diseases 1970–1980. Academic Press, London, pp 737–767
Carruthers RI, Soper RS (1987) Fungal diseases. In: Fuxa JR, Tanada Y (eds) Epizootiology of insect diseases. Wiley, New York
Chandler D, Hay D, Reid AP (1997) Sampling and occurrence of entomopathogenic fungi and nematodes in UK soils. Appl Soil Ecol 5:133–141
Charnley AK, St Leger RJ (1991) The role of cuticle-degrading enzymes in fungal pathogenesis in insects. In: Cole GT, Hoch MC (eds) The fungal spore and disease initiation in plants and animals. Plenum, New York, pp 267–286
Cherry AJ, Abalo P, Hell K (2005) A laboratory assessment of the potential of different strains of the entomopathogenic fungi Beauveria bassiana (Balsamo) Vuillemin and Metarhizium anisopliae (Metschnikoff) to control Callosobruchus maculatus (F.) (Coleoptera: Bruchidae) in stored cowpea. J Stored Prod Res 41:295–309
Clarkson JM, Charnley AK (1996) New insights into the mechanisms of fungal pathogenesis in insects. Trends Microbiol 4:197–203
Commission European (1991) Council directive 91/414/EEC of 15 July 1991 concerning the placing of plant protection products on the market. Off J Eur Commun L 230:1–32
Cox PD, Wilkin DR (1996) The potential use of biological control of pests of stored grain. Home-Grown cereals authority research review (36), HGCA, London, UK, p 53
Crespo R, Juárez MP, Dal Bello GM, Padín S, Fernández GC, Pedrini N (2002) Increased mortality of Acanthoscelides obtectus by alkane-grown Beauveria bassiana. Biocontrol 47:685–696
Dal Bello G, Padín S, Lastra CL, Fabrizio M (2001) Laboratory evaluation of chemical-biological control of the rice weevil (Sitophilus oryzae L.) in stored grains. J Stored Prod Res 37:77–84
Dal Bello G, Padín S, Juárez P, Pedrini N, De Giusto M (2006) Biocontrol of Acanthoscelides obtectus and Sitophilus oryzae with diatomaceous earth and Beauveria bassiana on stored grains. Biocontrol Sci Technol 16:215–220
Daoust RA, Roberts DW (1983) Studies on prolonged storage of Metarhizium anisopliae conidia: effect of temperature and relative humidity on conidial viability and virulence against mosquitoes. J Invertebr Pathol 41:143–150
De Faria MR, Wraight SP (2007) Mycoinsecticides and mycoacaricides: a comprehensive list with worldwide coverage and international classification of formulation types. Biol Control 43:237–256
Ekesi S, Maniania NK, Ampong-Nyarko K (1999) Effect of temperature on germination, radial growth and virulence of Metarhizium anisopliae and Beauveria bassiana on Megalurpthrups sjostedti. Biocontrol Sci Technol 9:177–185
Ekesi S, Akpa AD, Onu I (2000) Relative pathogenicity of different entomopathogenic fungi to Sitotroga cerealella in stored sorghum. Trop Sci 40:206–210
Ekesi S, Egwurube EA, Akpa AD, Onu I (2001) Laboratory evaluation of the entomopathogenic fungus, Metarhizium anisopliae for the control of the groundnut bruchid, Caryedon serratus on groundnut. J Stored Prod Res 37:313–321
Fargues J, Goettel MS, Smits N, Oudragogo A, Rougier M (1997) Effect of temperature on vegetative growth of Beauveria bassiana isolates from different origins. Mycologia 89:383–392
Ferron P (1977) Influence of relative humidity on the development of fungal infection caused by Beauveria bassiana (Fungi imperfecti, Moniliales) in imagines of Acanthoscelides obtectus (Coleoptera: Bruchidae). Entomophaga 22:393–396
Fields P, Subramanyam Bh, Hulasare R (2012) Extreme temperatures. In: Hagstrum DW, Phillips TW, Cuperus G (eds) Stored Product Protection, Kansas State University, p 351
Flanders SE (1930) Recent developments in Trichogramma production. J Econ Entomol 23:837–841
Flinn PW, Scholler M (2012) Biological control: Insect pathogens, parasitoids, and predators. In: Hagstrum DW, Phillips TW, Cuperus G (eds) Stored product protection. S156. Kansas State University, Manhattan, KS, pp 203–212
Froggatt WW (1912) Parasitic enemies of the mediterranean flour moth Ephestia kuehniella, Zeller. Agric Gaz N S W 23:307–311
Goettel MS, Inglis GD (1997) Fungi: hyphomycetes. In: Lacey LA (ed) Manual of techniques in insect pathology, vol 5–3. Academic Press, San Diego, pp 213–248
Hagstrum DW, Flinn PW (1995) Integrated pest management. In: Subramanyam Bh, Hagstrum DW (eds) Integrated management of insects in stored products. Marcel Dekker Inc, New York, pp 399–408
Hajek AE, St Leger RJ (1994) Interactions between fungal pathogens and insect hosts. Annu Rev Entomol 39:293–322
Han JH, Jin BR, Kim JJ, Lee SY (2014) Virulence of entomopathogenic fungi Metarhizium anisopliae and Paecilomyces fumosoroseus for the microbial control of Spodoptera exigua. Biol Control 42:385–390
Hansen LS, Steenberg T (2007) Combining larval parasitoids and an entomopathogenic fungus for biological control of Sitophilus granarius (Coleoptera: Curculionidae) in stored grain. Biol Control 40:237–242
Hedgecock S, Moore D, Higgins PM, Prior C (1995) Influence of moisture content on temperature tolerance and storage on Metarhizium flavoviride conidia in an oil formulation. Biocontrol Sci Technol 5:371–377
Hidalgo E, Moore D, Le Patoure G (1998) The effect of different formulations of Beauveria bassiana on Sitophilus zeamais in stored maize. J Stored Prod Res 34:171–179
Hluchý M, Samšiňáková A (1989) Comparative study on the susceptibility of adult Sitophilus granarius (L.) (Coleoptera: Curculionidae) and larval Galleria mellonella (L.) (Lepidoptera: Pyralidae) to the entomogenous fungus Beauveria bassiana (Bals.) Vuill. J Stored Prod Res 25:61–64
Hong TD, Jenkins NE, Ellis RH, Moore D (1998) Limits to the negative logarithmic relationship between moisture content and longevity in conidia of Metarhizium flavoviride. Ann Bot 81:625–630
Horaczek A, Viernstein H (2004) Comparison of three commonly used drying technologies with respect to activity and longevity of aerial conidia of Beauveria brongniartii and Metarhizium anisopliae. Biol Control 31:65–71
Hunter DK (1970) Pathogenicity of a granulosis virus of the Indian meal moth. J Invertebr Pathol 16:339–341
Inglis GD, Goettel MS, Butt TM, Strasser H (2001) Use of hyphomycetous fungi for managing insect pests. In: Butt TM, Jackson C, Magan N (eds) Fungi as biocontrol agents. Progress, problems and potential. CABI Publishing, Wallingford, pp 23–69
JrA Moino, Alves SB, Pereira RM (1998) Efficacy of Beauveria bassiana (Balsamo) Vuillemin isolates for control of stored-grain pests. J Appl Entomol 122:301–305
Kassa A, Zimmermann G, Stephan D, Vidal S (2002) Susceptibility of Sitophilus zeamais (Motsch.) (Coleoptera: Curculionidae) and Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae) to entomopathogenic fungi from Ethiopia. Biocontrol Sci Technol 12:727–736
Kavallieratos NG, Athanassiou CG, Pashalidou FG, Andris NS, Tomanović Z (2005) Influence of grain type on the insecticidal efficacy of two diatomaceous earth formulations against Rhyzopertha dominica (F) (Coleoptera: Bostrychidae). Pest Manag Sci 61:660–666
Kavallieratos NG, Athanassiou CG, Michalaki MP, Batta YA, Rigatos HA, Pashalidou FG, Balotis GN, Tomanović Z, Vayias BJ (2006) Effect of the combined use of Metarhizium anisopliae (Metschinkoff) Sorokin and diatomaceous earth for the control of three stored-product beetle species. Crop Prot 25:1087–1094
Kavallieratos NG, Wakefield ME, Athanassiou CG (2008) Factors affecting the attachment of conidia of Metarhizium anisopliae (Metschnikoff) Sorokin (Deuteromycotina: Hyphomycetes) to different body parts of Tribolium confusum Jacquelin du Val (Coleoptera: Tenebrionidae) adults. IOBC/WPRS Bull 40:181–190
Kavallieratos NG, Athanassiou CG, Aountala M, Kontodimas DC (2014) Evaluation of the entomopathogenic fungi Beauveria bassiana, Metarhizium anisopliae, and Isaria fumosorosea for control of Sitophilus oryzae. J Food Protect 77:87–93
Klingen I, Haukeland S (2006) The soil as a reservoir for natural enemies of pest insects and mites with emphasis on fungi and nematodes. In: Eilenberg J, Hokkanen HMT (eds) An ecological and societal approach to biological control. Springer, Dordrecht, pp 145–211
Lacey LA, Fransen JJ, Carruthers R (1996) Global distribution of naturally occurring fungi of Bemisia, their biologies and use as biological control agents. In: Gerling D, Mayer R (eds) Taxonomy, biology, damage, control and management. Intercept, Andover, pp 401–433
Lord JC (2001) Desiccant dusts synergise the effect of Beauveria bassiana (Hyphomycetes: Moniliales) on stored-grain beetles. J Econ Entomol 94:367–372
Lord JC (2003) Mattesia oryzaephili (Neogregarinorida: Lipotrophidae), a pathogen of stored-grain insects: virulence, host range and comparison with Mattesia dispora. Biocontrol Sci Technol 13:589–598
Lord JC (2005) Low humidity, moderate temperature, and desiccant dust favor efficacy of Beauveria bassiana (Hyphomycetes: Moniliales) for the lesser grain borer, Rhyzopertha dominica (Coleoptera: Bruchidae). Biol Control 34:180–186
Lord JC (2007a) Enhanced efficacy of Beauveria bassiana for red flour beetle with reduced moisture. J Econ Entomol 100:1071–1074
Lord JC (2007b) Desiccation increases the efficacy of Beauveria bassiana for stored-grain pest insect control. J Stored Prod Res 43:535–539
Lord JC (2009a) Beauveria bassiana infection of eggs of stored-product beetles. Entomol Res 39:155–157
Lord JC (2009b) Efficacy of Beauveria bassiana for control of Tribolium castaneum with reduced oxygen and increased carbon dioxide. J Appl Entomol 133:101–107
Lord JC, Campbell JF, Sedlacek JD, Vail PV (2007) Application and evaluation of entomopathogens for managing insects in stored products. In: Lacey LA, Kaya HK (eds) Field manual of techniques in invertebrate pathology. Springer, Dordrecht, pp 677–693
Mahdneshin Z, Safaralizadah MH, Ghosta Y (2009) Study on the efficacy of Iranian isolates of Beauveria bassiana (Balsamo) Vuillemin and Metarhizium anisopliae (Metsch.) Sorokin against Rhyzopertha dominica F. (Coleoptera: Bostrychidae). J Biol Sci 9:170–174
Mason LJ, McDonough M (2012) Biology, behavior, and ecology of stored grain and legume insects. In: Hagstrum DW, Phillips TW, Cuperus G (eds) Stored product protection. S156. Kansas State University, Manhattan, KS, pp 7–20
Mbata GN, Shapiro-Ilan DI (2005) Laboratory evaluation of virulence of Heterorhabditid nematodes to Plodia interpunctella Hübner (Lepidoptera:Pyralidae). Environ Entomol 34:676–682
Meikle WG, Cherry AJ, Holst N, Hounna B, Markham RH (2001) The effects of an entomopathogenic fungus, Beauveria bassiana (Balsamo) Vuillemin (Hyphomycetes), on Prostephanus truncatus (Horn) (Col.: Bostrichidae), Sitophilus zeamais Motschulsky (Col.: Curculionidae), and grain losses in stored maize in the Benin Republic. J Invertebr Pathol 77:198–205
Meyling NV, Eilenberg J (2007) Ecology of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae in temperate agroecosystems: Potential for conservation biological control. Biol Control 43:145–155
Michalaki M, Athanassiou CG, Kavallieratos NG, Batta YA, Balotis GN (2006) Effectiveness of Metarhizium anisopliae (Metschinkoff) Sorokin applied alone or in combination with diatomaceous earth against Tribolium confusum Jacquelin du Val: influence of temperature, relative humidity and type of commodity. Crop Prot 25:418–425
Michalaki MP, Athanassiou CG, Steenberg T, Buchelos CTh (2007) Effect of Paecilomyces fumosoroseus (Wise) Brown and Smith (Ascomycota: Hypocreales) alone or in combination with diatomaceous earth against Tribolium confusum Jacquelin du Val (Coleoptera: Tenebrionidae) and Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). Biol Control 40:280–286
Moore D, Higgins PM (1997) Viability of stored conidia of Metarhizium flavoviride Gams and Rozsypal, produced under different culture regimes and stored with clays. Biocontol Sci Technol 7:335–343
Moore D, Douro-Kpindou OK, Jenkins NE, Lomer CJ (1996) Effects of moisture content and temperature on storage of Metarhizium flavoviride conidia. Biocontrol Sci Technol 6:51–61
Moore D, Lord JC, Smith SM (2000) Pathogens. In: Subramanyam Bh, Hagstrum DW (eds) Alternatives to pesticides in stored product IPM. Kluwer Academic Publishers, Dordrecht, pp 193–227
Nansen C, Barton LEE, Nansen M (2007) Uptake, retention, and repellency of a potential carrier of active ingredients in crack and crevice treatments for stored-grain beetles. J Stored Prod Res 43:417–424
Nboyine JA, Asante SK, Nutsugah SK, Abudulai M, Ansaah-Agyapong F, Luke B, Clottey V (2015) Biological control of the larger grain borer, Prostephanus truncatus (Horn) in stored maize using the fungal pathogen, Beauveria bassiana and the predator Teretrius nigrescens Lewis. J Stored Prod Postharvest Res 6:30–37
Negrisoli CRDCB, Negrisoli ASJ, Bernardi D, Garcia MS (2013) Activity of eight strains of entomopathogenic nematodes (Rhabditida: Steinernematidae, Heterorhabditidae) against five stored product pests. Exp Parasitol 134:384–388
Nouri-Ganbalani G, Borzoui E, Abdolmaleki A, Abedi Z, Kamita SG (2016) Individual and combined effects of Bacillus thuringiensis and azadirachtin on Plodia interpunctella Hübner (Lepidoptera: Pyralidae). J Insect Sci 16:95
Oduor GI, Smith SM, Chandi EA, Karanja LW, Agano JO, Moore D (2000) Occurrence of Beauveria bassiana on insect pests of stored maize in Kenya. J Stored Prod Res 36:177–185
Oppert B, Morgan TD, Kramer KJ (2011) Efficacy of Bacillus thuringiensis Cry3Aa protoxin and protease inhibitors against coleopteran storage pests. Pest Manag Sci 67:568–573
Ortiz-Urquiza A, Keyhani NO (2013) Action on the surface: entomopathogenic fungi versus the insect cuticle. Insects 4:357–374
Ortiz-Urquiza A, Keyhani NO (2016) Molecular genetics of Beauveria bassiana infection of insects. In: Lovett B, St Leger RJ (eds) Genetics and molecular biology of entomopathogenic fungi. Elsevier Inc, Oxford, pp 165–249
Padín SB, Dal-Bello G, Vasicek AL (1997) Pathogenicity of Beauveria bassiana for adults of Tribolium castaneum (Coleoptera, Tenebrionidae) in stored-grains. Entomophaga 42:569–574
Padín SB, Dal Bello G, Fabrizio M (2002) Grain loss caused by Tribolium castaneum, Sitophilus oryzae and Acanthoscelides obtectus in stored durum wheat and beans treated with Beauveria bassiana. J Stored Prod Res 38:69–74
Pedrini N, Ortiz-Urquiza A, Huarte-Bonnet C, Fan Y, Juárez MP, Keyhani NO (2015) Tenebrionid secretions and a fungal benzoquinone oxidoreductase form competing components of an arms race between a host and pathogen. Proc Natl Acad Sci USA 112:E3651–E3660
Pilz C, Wegensteiner R, Keller S (2008) Natural occurrence of insect pathogenic fungi and insect parasitic nematodes in Diabrotica virgifera virgifera populations. Biocontrol 53:353–359
Prior C (1991) Discovery and characterization of fungal pathogens for locust and grasshopper control. In: Lomer CJ, Prior C (eds) Biological control of locusts and grasshoppers. CAB International, Wallingford, pp 159–179
Quesada-Moraga E, Navas-Cortés JA, Maranhao EAA, Ortiz-Urquiza A, Santiago-Álvarez C (2007) Factors affecting the occurrence and distribution of entomopathogenic fungi in natural and cultivated soils. Mycol Res 111:947–966
Ramaswamy K, Vijayarangan N, Krishnaiah HE (2009) Insecticidal effect of Beauveria bassiana and Paecilomyces fumosoroseus alone and in combination with diatomaceous earth against rice weevil (Sitophilus oryzae) and red flour beetle (Tribolium castaneum). J Pure Appl Microbiol 3:637–642
Riasat T, Wakil W, Ashfaq M, Sahi ST (2011) Effect of Beauveria bassiana mixed with diatomaceous earth on mortality, mycosis and sporulation of Rhyzopertha dominica on stored wheat. Phytoparasitica 39:325–331
Rice WC, Cogburn RR (1999) Activity of the entomopathogenic fungus Beauveria bassiana (Deuteromycota: Hyphomycetes) against three coleopteran pests of stored grain. J Econ Entomol 92:691–694
Roberts DW, Campbell AS (1977) Stability of entomopathogenic fungi. Misc Publ Entomol Soc Am 10:19–76
Rodrigues C, Pratissoli D (1990) Pathogenicity of Beauveria brongniartii (Sacc.) Petch. and Metarhizium anisopliae (Mols.) Sorok. and its affect on corn weevil and bean beetle. Ann Entomol Soc Braz 19:302–306
Rodríguez-Gómez D, Loera O, Saucedo-Castañeda G, Viniegra-González G (2009) Substrate influence on physiology and virulence of Beauveria bassiana acting on larvae and adults of Tenebrio molitor. World J Microbiol Biotechnol 25:513–518
Rumbos CI, Athanassiou CG (2012) Insecticidal effect of six entomopathogenic nematode strains against Lasioderma serricorne (F.) (Coleoptera: Anobiidae) and Tribolium confusum Jacquelin du Val (Coleoptera: Tenebrionidae). J Stored Prod Res 50:21–26
Rumbos CI, Athanassiou CG (2016) The use of entomopathogenic nematodes in the control of stored-product insects. J Pest Sci. doi:10.1007/s10340-016-0795-y
Ryabov MA (1926) The possibilities of applying the parasitic method of control in the case of granary pests. Bull North Cauc Plant Prot Stn 1:19–50
Safavi SA, Shah FA, Pakdel AK, Rasoulian GR, Bandani AR, Butt TM (2007) Effect of nutrition on growth and virulence of the entomopathogenic fungus Beauveria bassiana. FEMS Microbiol Lett 270:116–123
Saik JE, Lacey LA, Lacey CM (1990) Safety of microbial insecticides to vertebrates—domestic animals and wildlife. In: Laird M, Lacey LA, Davidson FW (eds) Safety of microbial insecticides. CRC Press, Boca Raton, pp 115–132
Sánchez-Pena SR, Lara JSJ, Medina RF (2011) Occurrence of entomopathogenic fungi from agricultural and natural ecosystems in Saltillo, Mexico, and their virulence towards thrips and whiteflies. J Insect Sci 11:1–10
Schöller M, Prozell S, Al-Kirshi A-G, Reichmuth Ch (1997) Towards biological control as a major component of integrated pest management in stored product protection. J Stored Prod Res 33:81–97
Searle T, Doberski J (1984) An investigation of the entomogenous fungus Beauveria bassiana (Bals.) Vuill. as a potential biological control agent for Oryzaephilus surinamensis (L.). J Stored Prod Res 20:17–23
Shafighi Y, Ziaee M, Ghosta Y (2014) Diatomaceous earth used against insect pests, applied alone or in combination with Metarhizium anisopliae and Beauveria bassiana. J Plant Prot Res 33:81–97
Sheeba G, Seshadri S, Raja N, Janarthanan S, Ignacimuthu S (2001) Efficacy of Beauveria bassiana for control of the rice weevil Sitophilus oryzae (L.) (Coleoptera: Curculionidae). Appl Entomol Zool 36:117–120
Siegel JP, Shadduck JA (1990) Safety of microbial insecticides to vertebrates-humans. In: Laird M, Lacey LA, Davidson EW (eds) Safety of microbial insecticides. CRC Press, Boca Raton, pp 101–113
Smith RJ, Grula EA (1981) Nutritional requirements for conidial germination and hyphal growth of Beauveria bassiana. J Invertebr Pathol 37:222–230
Smith SM, Oduor GI, Moore D (1998) Preliminary investigations into the potential of entomopathogenic fungi for the control of pests of stored maize. In: Smith PH (ed) Insect pathogens and insect parasitic nematodes. Bulletin OILB/SROP, vol 21, pp 53–60
Smith SM, Moore D, Karanja LW, Chandi EA (1999) Formulation of vegetable fat pellets with pheromone and Beauveria bassiana to control the larger grain borer, Prostephanus truncatus (Horn). Pesticide Sci 55:711–718
Smith SM, Moore D, Oduor GI, Wright DJ, Chandi EA, Agano JO (2006) Effect of wood ash and conidia of Beauveria bassiana (Balsamo) Vuillemin on mortality of Prostephanus truncatus (Horn). J Stored Prod Res 42:357–366
Soper R (1978) Autodissemination of entomopathogens: fungi. In: Allen GE, Ignoffo CM, Jaques RP (eds) Future strategies in pest management systems. Proceedings of the National Science Foundation, United States Department of Agriculture and the University of Florida Workshop on Microbial Control of Insect Pests, Gainesville, FL, pp 63–65
Sosa-Gomez DR, Boucias DG, Nation JL (1997) Attachment of Metarhizium anisopliae to the southern green stinkbug Nezara viridula cuticle and fungistatic effect of cuticular lipids and aldehydes. J Invertebr Pathol 69:31–39
Srivastava CN, Maurya P, Sharma P, Mohan L (2009) Prospective role of insecticides of fungal origin: review. Entomol Res 39:341–355
Stephou VK, Tjamos SE, Paplomatas EJ, Athanassiou CG (2012) Transformation and attachment of Beauveria bassiana conidia on the cuticle of Tribolium confusum and Sitophilus oryzae in conjunction with diatomaceous earth. J Pest Sci 85:387–394
Storm C, Scoates F, Nunn A, Potin O, Dillon A (2016) Improving efficacy of Beauveria bassiana against stored grain beetles with a synergistic co-formulant. Insects 7:42
Subramanyam Bh, Hagstrum DW (1995) Integrated management of insects in stored products. Marcel Dekker Inc, New York, p 408
Throne JE (1989) Effects of noncatastrophic control technologies that alter life history parameters on insect population growth: a simulation study. Environ Entomol 18:1050–1055
Throne JE, Lord JC (2004) Control of sawtoothed grain beetles (Coleoptera: Silvanidae) in stored oats by using an entomopathogenic fungus in conjunction with seed resistance. J Econ Entomol 97:1765–1771
Trematerra P, Athanassiou CG, Sciarretta A, Kavallieratos NG, Buchelos CTh (2013) Efficacy of the auto-confusion system for mating disruption of Ephestia kuehniella (Zeller) and Plodia interpunctella (Hübner). J Stored Prod Res 55:90–98
Vail PV, Tebbets JS, Cowan DC, Jenner KE (1991) Efficacy and persistance of a granulosis virus against infestations of Plodia interpunctella (Hübner) (Lepidoptera: Pyralidae) on raisins. J Stored Prod Res 27:103–107
Varela JA, Morales E (1996) Characterization of some Beauveria bassiana isolates and their virulence toward the coffee berry borer Hypothenemus hampei. J Invertebr Pathol 67:147–152
Vassilakos TN, Athanassiou CG, Kavallieratos NG, Vayias BJ (2006) Influence of temperature on the insecticidal effect of Beauveria bassiana in combination with diatomaceous earth against Rhyzopertha dominica and Sitophilus oryzae on stored wheat. Biol Control 38:270–281
Vestergaard S, Butt TM, Bresciani J, Gillespie AT, Eilenberg J (1999) Light and electron microscopy studies of the infection of the western flower thrips Frankliniella occidentalis (Thysanoptera: Thripidae) by the entomopathogenic fungus Metarhizium anisopliae. J Invertebr Pathol 73:25–33
Wakefield ME (2006) Factors affecting storage insect susceptibility to the entomopathogenic fungus Beauveria bassiana. In: Proceedings of the 9th international working conference on stored product protection, 15–18 October 2006, Campinas, Sao Paolo, Brazil, pp 855–862
Wakefield ME, Moore D, Luke B, Taylor B, Storm CG, Collins DA, Grammare P, Potin O (2010) Progress in the development of a biopesticide for the structural treatment of grain stores. In: Proceedings of the 10th international working conference on stored product protection, 27 June–2 July 2010, Estoril, Portugal, pp 760–765
Wakil W, Schmitt T (2015) Field trials on the efficacy of Beauveria bassiana, diatomaceous earth and Imidacloprid for the protection of wheat grains from four major stored grain insect pests. J Stored Prod Res 64:160–167
Wakil W, Riasat T, Ghazanfar MU, Kwon YJ, Shaheen FA (2011) Aptness of Beauveria bassiana and enhanced diatomaceous earth (DEBBM) for control of Rhyzopertha dominica F. Entomol Res 41:233–241
Wakil W, Riasat T, Ashfaq M (2012) Residual efficacy of thiamethoxam, Beauveria bassiana (Balsamo) Vuillemin, and diatomaceous earth formulation against Rhyzopertha dominica F. (Coleoptera: Bostrychidae). J Pest Sci 85:341–350
Walstad JD, Anderson RF, Stambaugh WJ (1970) Effects of environmental conditions on two species of muscardine fungus (Beauveria bassiana and Metarhizium anisopliae). J Invertebr Pathol 16:221–226
White NDG (1995) Insects, mites, and insecticides in stored grain ecosystems. In: Jayas DS, White NDG, Muir WE (eds) Stored-grain ecosystems. Marcel Dekker Inc., New York, pp 123–168
Wraight SP, Hajek AE (2009) Manipulation of arthropod pathogens for integrated pest management. In: Radcliffe EB, Hutchison WD, Cancelado RE (eds) Integrated pest management: concepts, tactics, strategies and case studies. Cambridge University Press, New York, pp 131–150
Wraight SP, Jackson MA, de Kock SL (2001) Production, stabilization, and formulation of fungal biocontrol agents. In: Butt TM, Jackson CW, Magan N (eds) Fungi as biocontrol agents: progress, problems and potential. CABI Publishing, Wallingford, pp 253–288
Xiao G, Ying S-H, Zheng P, Wang Z-L, Zhang S, Xie X-Q, Shang Y, St Leger RJ, Zhao G-P, Wang C, Feng M-G (2012) Genomic perspectives on the evolution of fungal entomopathogenicity in Beauveria bassiana. Sci Rep 2:483
Yilmaz S, Ayvaz A, Akbulut M, Azizoglu U, Karabörklü S (2012) A novel Bacillus thuringiensis strain and its pathogenicity against three important pest insects. J Stored Prod Res 51:33–40
Zettler JL, Arthur FH (2000) Chemical control of stored product insects with fumigants and residual treatments. Crop Prot 19:577–582
Zimmermann G (1986) The ‘Galleria bait method’ for detection of entomopathogenic fungi in soil. J Appl Entomol 102:213–215
Acknowledgements
We would like to thank Frank H. Arthur and James E. Throne for reading the manuscript prior to submission.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
Christos Rumbos and Christos Athanassiou declare that there have no conflicts of interest. Christos Rumbos and Christos Athanassiou conceived the work and wrote the manuscript.
Research involving animal and human rights
The research did not involve human participants and/or animals.
Ethical approval
This article does not contain any studies with human participants performed by any of the authors.
Additional information
Communicated by N. Desneux.
Rights and permissions
About this article
Cite this article
Rumbos, C.I., Athanassiou, C.G. Use of entomopathogenic fungi for the control of stored-product insects: can fungi protect durable commodities?. J Pest Sci 90, 839–854 (2017). https://doi.org/10.1007/s10340-017-0849-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10340-017-0849-9